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Politically, Verres initially supported Gaius Marius and the Populares, but soon went over to the Optimates. Sulla made him a present of land at Beneventum, and secured him against punishment for embezzlement. In 80 BC, Verres was legate in Asia on the staff of Gnaeus Cornelius Dolabella, governor of Cilicia. The governor and his subordinate plundered in concert until 78 BC, when Dolabella had to stand trial at Rome. He was found not guilty and acquitted.[8]

In 74, by lavish use of bribes, Verres secured the city praetorship. He abused his authority to further the political ends of his party. As a reward, he was then sent as governor to Sicily, the breadbasket of the Roman Republic and a particularly rich province thanks to its central position in the Mediterranean making it a commercial crossroads. The people were for the most part prosperous and contented, but under Verres, the island experienced more misery and desolation than during the time of the First Punic or the recent servile wars. The wheat-growers and the revenue collectors were ruined by exorbitant imposts or by the iniquitous canceling of contracts. Temples and private houses were robbed of their works of art and the rights of Roman citizens were disregarded.

Another major charge leveled against Verres during his Sicilian tenure was that, during the time of the Third Servile War against Spartacus, he had used the emergency to raise cash. He would, allegedly, pick key slaves of wealthy landowners and charge them with plotting to join Spartacus' revolt or otherwise causing sedition in the province. Having done so, he would sentence the slave to death by crucifixion, and then lay a broad hint that a sizable bribe from the slave's owner could expunge the charge and sentence. Other times he would name non-existent slaves, charging that the landowner held a slave that was suspected of plotting rebellion and that the owner was actively hiding him. When the owner, quite understandably, could not produce the slave (which he didn't own), Verres would throw him in prison until a bribe could be paid for the landowner's release.

Verres returned to Rome in 70, and in the same year, at the request of the Sicilians, Marcus Tullius Cicero prosecuted him: the prosecution speeches were later published as the Verrine Orations. Verres entrusted his defence to the most eminent of Roman advocates, Quintus Hortensius, and he had the sympathy and support of several of the leading Roman patricians.

The court was composed exclusively of senators, some of whom may have been his friends. However, the presiding judge, the city praetor, Manius Acilius Glabrio, was a thoroughly honest man, and his assessors were at least not accessible to bribery. Verres vainly tried to get the trial postponed until 69 when his friend Marcus Caecilius Metellus would be the presiding judge. Hortensius tried two successive tactics to delay the trial. The first was trying to sideline Verres' prosecution by hoping to get a prosecution of a former governor of Bithynia to take precedence. When that failed, the defense then looked to procedural delays (and gaming the usual format of a Roman extortion trial) until after a lengthy and upcoming round of public holidays, after which there would be scarce time for the trial to continue before Glabrio's term was up and the new and more malleable judge would be installed. However, in August, Cicero opened the case and vowed to short-circuit the plans by taking advantage of an opportunity to change the format of the trial to bring evidence and witnesses up much sooner, and opened his case with a short and blistering speech.

The effect of the first brief speech was so overwhelming that Hortensius refused to reply, and recommended his client leave the country. Before the expiration of the 9 days allowed for the prosecution Verres was on his way to Massilia (today Marseille). There he lived in exile until 43 BC, when he was proscribed by Mark Antony, apparently for refusing to surrender some art treasures that Antony coveted.

Verres may have had a more decent character than that with which Cicero, the primary source of information, credits him, but there is no evidence to counter the allegation that he stood preeminent among the worst specimens of Roman provincial governors. Of the seven Verrine orations, only two were delivered; the remaining five were compiled from the depositions of witnesses and published after Verres' flight.

Verres is a major character in the novel Spartacus: Swords and Ashes by Jonathan Clements, which is set on the eve of his governorship of Sicily and concerns an undocumented dispute with a young Cicero in Neapolis.

In Fortune's Favourites by Colleen McCullough, Verres, while a secondary character, describes his career in detail, since his pillaging of the Samnium during the Social War, from his departure to Asia in the retinue of governor Gnaeus Cornelius Dolabella, where the author describes his vices and immensurable greed, foreshadowing his misgovernment of Sicily, and, in the end, Cicero's energic prosecution.